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Termite's Twisted Mandible Presents Fast, Powerful, and Precise Strikes

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Termite's Twisted Mandible Presents Fast, Powerful, and Precise Strikes www.nature.com/scientificreports OPEN Termite’s Twisted Mandible Presents Fast, Powerful, and Precise Strikes Kuan-Chih Kuan1,5, Chun-I Chiu1,5, Ming-Chih Shih2, Kai-Jung Chi2,3,4 ✉ & Hou-Feng Li1 ✉ The asymmetric mandibles of termites are hypothetically more efcient, rapid, and powerful than the symmetric mandibles of snap-jaw ants or termites. We investigated the velocity, force, precision, and defensive performance of the asymmetric mandibular snaps of a termite species, Pericapritermes nitobei. Ultrahigh-speed recordings of termites revealed a new record in biological movement, with a peak linear velocity of 89.7–132.4 m/s within 8.68 μs after snapping, which caused an impact force of 105.8–156.2 mN. High-speed video recordings of ball-strike experiments on termites were analysed using the principle of energy conservation; the left mandibles precisely hit metal balls at the left-to- front side with a maximum linear velocity of 80.3 ± 15.9 m/s (44.0–107.7 m/s) and an impact force of 94.7 ± 18.8 mN (51.9–127.1 mN). In experimental fghts between termites and ant predators, Pe. nitobei killed 90–100% of the generalist ants with a single snap and was less likely to harm specialist ponerine ants. Compared with other forms, the asymmetric snapping mandibles of Pe. nitobei required less elastic energy to achieve high velocity. Moreover, the ability of P. nitobei to strike its target at the front side is advantageous for defence in tunnels. Some invertebrates’ elastic power-amplifying systems that incorporate latches and springs can overcome the physiological limits of muscle contraction and perform a powerful or rapid movement1,2. For example, mantis shrimps (Crustacea: Stomatopoda) perform high-speed strikes to prey by using elastic energy stored in their raptorial appendages3. Springtails (Hexapoda: Collembola) escape from enemies with quick and powerful jumps by using their springing organ4. Many ants and termites, such as the snap-jaw ant Mystrium camillae Emery (Hymenoptera: Formicidae)5 and the soldiers of termite Termes panamaensis (Snyder) (Blattodea: Termitidae)6, have mandibles that are morphologically specialised for powerful snapping attacks. Te snapping speeds of the mandibular attacks of M. camillae (111.1 m/s)5 and T. panamaensis (67 m/s)6 are the most rapid animal move- ments currently reported1,5,6, followed by the mandible-closing movement of Odontomachus bauri Emery trap-jaw ants (64.3 m/s)7, the diving of gyrfalcons (58 m/s)8, the nematocyst discharge of jellyfsh (37 m/s)9, and strike behaviour of mantis shrimps (31 m/s)1. Te snapping mandibles of termite soldiers have two forms: symmetric and asymmetric10,11. T. panamaensis has two narrow and elongated symmetric snapping mandibles that press together until they slide against each other (Fig. 1a). Tese mandibles strike enemies along their lateral sides6. By contrast, the asymmetric snapping mandibles of some termites are relatively short and wide, with a twisted lef mandible and curved right mandi- ble10. Te right mandible presses against the lef until the two surfaces slide. Moreover, the lef mandible snaps in a clockwise motion (Fig. 1b), presumably striking enemies along the front side. Additionally, asymmetric snapping mandibles may perform more violent strikes than symmetric mandibles can by storing elastic energy in the lef twisted mandible12. However, no conclusive evidence has supported these hypotheses. Ants are major natural predators of termites. Predator ants include specialist predators such as Pachycondyla spp. (Formicidae: Ponerinae)13 and generalist predators such as Anoplolepis spp. and Pheidole spp.14,15. Te power- ful mandibular snapping of termite soldiers is hypothesised to be a specialised defence mechanism against ants16. Termites can snap the ground to leap away from ants17,18 or snap at ants to push them away16 or even kill them6. However, these defensive behaviours have not been studied in termites with asymmetric mandibles. 1Department of Entomology, National Chung Hsing University, Taichung City, Taiwan. 2Department of Physics and Institute of Biophysics, National Chung Hsing University, Taichung City, Taiwan. 3Department of Life Sciences, National Chung Hsing University, Taichung City, Taiwan. 4The iEGG and Animal Biotechnology Center, National Chung Hsing University, Taichung City, Taiwan. 5These authors contributed equally: Kuan-Chih Kuan and Chun-I Chiu. ✉e-mail: [email protected]; [email protected] SCIENTIFIC REPORTS | (2020) 10:9462 | https://doi.org/10.1038/s41598-020-66294-1 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. Snapping mandibles of termite soldiers. (a) In the symmetric snapping of Termes panamaensi6,10, elastic energy is stored in both mandibles, as indicated by the deformation and motion of the lef (L) and right (R) mandibles. (b) In the asymmetric snapping of Pericapritermes spp.10, elastic energy is stored in only the lef mandible when its anterior part rotates about the joint or pivot point O. Te posterior part remains stationary during snapping. (c) Morphology of the twisted lef mandible of the Pericapritermes nitobei termite used in this study. Te length of the anterior part of the lef mandible (LA) and the mass of its subsections A1 and A2 (i.e., MA1, MA2) are required to estimate its moment of inertia (IA). Te subsections A1 and A2 were prepared by performing two cuts; one cut was made at the pivot point (C1) and the other was made at the centre of the anterior part (C2). Tis study investigated the velocity, force, precision, and defensive behaviours of asymmetric mandibu- lar snaps performed by Pericapritermes nitobei (Shiraki) soldiers. Specifcally, we conducted ultrahigh- and high-speed video recordings, ball-strike experiments, and ant-defence assessments to test the following hypoth- eses: (1) snaps of asymmetric mandibles are more rapid and powerful than snaps of symmetric mandibles are, (2) asymmetric mandibles can precisely strike at the front side, and (3) asymmetric mandibles are efective for defending against ants. In addition to revealing the fastest known animal movement, we compared asymmetric and symmetric termite mandibles and analysed the evolution and mechanical efects of mandible morphology. Methods Termites and ants. A total of 100 Pe. nitobei termite soldiers were collected by excavating the soil beneath stones and logs in three locations in Taiwan, namely Xiaping Tropical Botanical Garden (23.77°N, 120.67°E), Huisun Forest Station (24.09°N, 121.03°E), and Dakeng (24.19°N, 120.79°E) (Supplementary Information, Table S1). Pe. nitobei is a soil-feeding termite that does not have a centralised nest; they distribute their eggs and larvae in subterranean tunnels beneath stones19. Tey generally forage on organic matter adjacent to plant roots and rarely appear on the ground surface19. Because Pe. nitobei colonies are difcult to maintain in laboratory conditions, all experiments were conducted within 1 day afer collection. Te sample sizes and collection sites of subjects used in all the experiments are summarised in Table S1 of the Supplementary Information. Natural predators of Pe. nitobei were identifed on the basis of references and feld observations. Pheidole and Anoplolepis spp. are generalist termite predators14,15, and Anochetus and Pachycondyla spp. are specialist predators of termites that perform specialised striking behaviours on termite soldiers or recognise termite odours and raid termite nests20,21. In this study, Ph. megacephala (Formicidae: Myrmecinae) and Anop. gracilipes (Formicidae: Formicinae) were assumed to be generalist predators of Pe. nitobei. Both species have been observed to for- age on the ground and prey on termites in Xiaping Tropical Botanical Garden22,23. Two ponerine ant species (Formicidae: Ponerinae), namely Anochetus taiwaniensis and Pa. javanus, were assumed to be specialist predators of Pe. nitobei. Anoc. taiwaniensis was observed foraging for termites in rotting logs at Huisun Forest Station. Pa. javanus was observed foraging in the soil surrounding the subterranean galleries of Pe. nitobei in Xiaping Tropical Botanical Garden, Huisun Forest Station, and Dakeng. Te generalist and specialist ants used in the assessments were collected from National Chung Hsing University and Huisun Forest Station, respectively (Supplementary Information, Table S1). SCIENTIFIC REPORTS | (2020) 10:9462 | https://doi.org/10.1038/s41598-020-66294-1 2 www.nature.com/scientificreports/ www.nature.com/scientificreports Estimating velocity and force by using an ultrahigh-speed camera. In each experiment, a termite was placed in the centre of a plastic petri dish (diameter: 90 mm) with a flter paper (Advantec No. 1, Toyo Inc.; diameter: 90 mm). Snapping behaviour was then recorded at 460,830 frames per second (fps) by using an ultrahigh-speed video camera (Model: v2512, Phantom, New Jersey, USA) with a resolution of 128 × 128 pixels2. Te linear velocity of the mandible tip (VMT) was calculated as follows: VLMT = AAω , (1) where LA and ωA are the length and angular velocity of the anterior rotating part about the pivot point O (Fig. 1c), respectively. Te parameter ωA was calculated from the video footage by using Phantom CV 2.8 (Phantom, New Jersey, USA) for image analysis. 6,7 Te snapping force (FA) was calculated using the following equation: 1 FMAA= LAAα , 3 (2) where MA and αA are the mass and angular acceleration of the anterior rotating part of the lef mandible, respec- tively. Te average αA can be calculated as follows: ωA αA = , tA (3) where tA is the time required to reach the maximum ωA. Te snapping energy (EA) (i.e., the kinetic energy due to rotation) was calculated as follows: 1 2 EIAA= ωA 2 (4) where IA is the moment of inertia of the anterior rotating part about the pivot point O (Fig. 1c). Because the ter- mite’s lef mandible cannot be modelled using a common geometrical form, we adjusted the moment of inertia (IA) by using a constant K as follows: 2 IKAA=.MLA (5) Te parameter K was calculated using the location of the anterior lef mandible’s centre of mass (LCOM), length of the anterior mandible part (LA), and mass of mandible parts A1 (MA1) and A2 (MA2) (Fig.
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